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Zeitschrift/Journal: Cicadina = Beiträge zur Zikadenkunde

Jahr/Year: 2011

Band/Volume: 12

Autor(en)/Author(s): Quartau Jose Alberto, Boieiro Mario, Rego Carla, Menezes Dilia, Goncalves Ysabel, Capela Ruben

Artikel/Article: Asianidia Zachvatkin (Hemiptera, Cicadellidae) associated with the laurisilva forest of island: species phenology and hostplant preferences. 47-56 Cicadina 12: 47-56 (2011)©Arbeitskreis Zikaden Mitteleuropas e.V. - download unter www.biologiezentrum.at 47

A sian idia Zachvatkin (Hemiptera, Cicadellidae) associated with the laurisilva forest of Madeira island: species phenology and host- preferences José Alberto Quartau1*, Mario Boieiro1, Carla Rego2, Dilia Menezes3, Ysabel Gonçalves4 & Rüben Capela5

Abstract: Five A sianidia Zachvatkin species (Hemiptera, Cicadellidae) A. albula, A . decolor, A . insulana, A . chiysanthemi and A . melliferae - were found in a survey o f the leafhoppers associated with a patch o f the laurel forest in Madeira island. A total of 513 specimens were collected as a result o f a two- year study. A sianidia decolor was the most abundant species (47%), followed by A . albula (36%) and A . insulana (16%). A . chiysanthemi and A . melliferae were scarcely found. These leafhoppers proved to be active mostly during spring and summer, but A . albula and A . decolor also showed a peak of abundance during November. The A sianidia species showed considerable variation in host-plant preferences, being some of them monophagous (A . chiysanthemi and A . melliferae), while others are oligophagous or even have a wide range of host- (A . albula, A . decolor and A . insulana). During this study new associations were found between these leafhoppers and plants o f the Madeiran laurisilva. The host-plant spectra of the closely related Asianidia albula and A . decolor showed considerable overlap. On the contrary, A . insulana, a species of a different lineage, had different host-plants. It is possible that differences in the preference for host-plants might have played a key role in the diversification o f A sianidia in the Madeiran laurisilva. Zusammenfassung: Im Rahmen einer Untersuchung zur Zikadenfauna von Lorbeerwäldern auf Madeira wurden fünf Arten der Gattung A sianidia Zachvatkin nachgewiesen: A . albula, A . decolor, A. insulana, A . chiysanthemi und A . melliferae. In Summe wurden 513 Individuen gesammelt. Die Häufigste Art war A sianidia decolor (47%), gefolgt von A . albula (36%) und A . insulana (16%). A . chiysanthemi und A . melliferae wurden nur in geringer Zahl gefangen. Die Hauptaktivität der Arten ist im Frühjahr und Sommer, A . albula und A . decolor zeigten ein weiteres Abundanzmaximum im November. A sianidia chiysanthemi und A . melliferae sind monophag, die anderen drei Arten oligo- bis polyphag.

1 Centro de Biología Ambiental/Departamento de Biología Animal, Faculdade de Ciéncias da Universidade de Lisboa, 1749-016 Lisboa, Portugal. 2Azorean Biodiversity Group (CITA-A), Departamento de Ciéncias Agrárias, Universidade dos Azores, 9700-042 Angra do Heroísmo, Terceira, Portugal. 3 Parque Natural da Madeira, Quinta do Bom Sucesso, Caminho do Meio, 9050-251 Funchal, Madeira, Portugal. 4 Museu Municipal do Funchal, Rúa da Mouraria 31, 9004-546 Funchal, Madeira, Portugal. 3 Centro de Estados da Macaronésia/Departamento de Biología, Universidade da Madeira, Campus da Perneada, 9000-390 Funchal, Madeira, Portugal. * Corresponding author. E-Mail: [email protected] 48 J. A. Quartau et©Arbeitskreis al. Zikaden Mitteleuropas e.V. - download unter www.biologiezentrum.at

Im Rahmen dieser Studie konnten neue Nährpflanzenassoziationen zwischen Asianidia-A rten und Pflanzenarten der Lorbeerwälder gefunden werden. Die Nährpflanzenspektren der nahe verwandten Arten A . albula und A . decolor zeigten große Ähnlichkeiten, während die systematisch weiter entferne A lt A . insulana andere Nährpflanzen nützt. Möglicherweise spielte die unterschiedliche Nahrungspräferenz eine entscheidende Rolle in Artbildungsprozesen der Gattung A sianidia auf Madeira. Kej' words: Leafhoppers, Asianidia, laurisilva, host-plants, Madeira

1. Introduction

The genus A sianidia Zachvatkin is represented in Madeira by nine species, six of which are stricdy endemic to this archipelago — A. albula, A. atlantica, A. chinai, A. insulana, A. madeirensis and A . melliferae (Quartau, 2007, 2008; Aguin-Pombo & Freitas, 2008). A similar situation exists in the , where 14 endemic species of A sianidia have been recorded (Lindberg, 1954; Oromi et. al., 2004). According to Quartau (1996), the high number of endemic A sianidia in Madeira, and in Macaronesia in general, may offer a good example of the adaptive radiation process by host-shift. For most phytophagous insects, plants provide not only a food source but also frequendy the bulk o f their environment, such as for concealment, substrate-borne communication during courtship, mating and oviposition (Claridge et al., 1997). So, differences in the preferences for the host-plants for feeding and/or ovipositing might have increasingly driven the establishment of patterns of specialization among some insect populations. Colonizing a new host and specializing in its resources could originate host races and eventually lead to speciation, particularly if the insects mate assortatively on their host (e.g., Bush & Butlin, 2004; Matsubayashi et al., 2010; Nyman, 2010). In fact, given enough time, these populations may diverge slowly by the adaptation to different host-species, thus becoming independent and distinct species through a sympatric process (Bernays & Chapman, 1994; Bush, 1994; Bush & Butlin, 2004). As such, host-plant differentiation would be a major factor in the initial origin of the new closely related species. Bush and Butlin (op.cit.), for instance, pointed out that sympatric divergence due to host-shift could be the major source of diversity in many phytophagous and parasitoid insects, groups that are particularly speciose. During the last decades some studies have shown that species once thought to be polyphagous are instead genetically differentiated groups of specialized populations. Some of these groups are differentiated populations still capable o f interbreeding, while others are sympatric species adapted to different host plants or complexes of sibling species (Thompson, 1994). In what concerns the A sianidia species, these exhibit a considerable diversity in their host specificity. As typical typhlocybines they feed not by sucking sap, like most other leafhoppers, but mostly by emptying the leaf mesophyll cells of their contents, so that a whitish stippling can be visible on the leaves as a result of their feeding activity (e.g., DeLong, 1971). Some species have been found on several host-plant species (even from different families), while others are extremely specific in host utilization, having been observed exclusively in one plant species, such as A . chinai and A . melliferae, in relation to Isoplexis sceptrum and Euphorbia mellifera, respectively (Quartau, 1996). Nevertheless, no definite conclusions can be drawn regarding the ecological niches for each o f the Madeiran A sianidia species, since for most of these leafhoppers the range of the host- Asianidia©Arbeitskreis Zachvatkin Zikaden Mitteleuropasassociated e.V. with - download the laurisilva unter www.biologiezentrum.at forest of Madeira island 49

plants for feeding and ovipositing, for instance, is far from being properly known. Host preferences are difficult to determine since most habitats where A sianidia occur can include a mixture o f a high number o f vascular plants, namely a great diversity of herbaceous species. Moreover, it is well known that leafhoppers are also able of performing vertical migrations from the herbaceous vegetation up to the plant canopy (Nickel et al., 2002), thus making difficult the complete inventory of their hosts. The recent data by Quartau (1996, 2007 and 2008) and Quartau & Remane (1996) on the Madeiran leafhoppers served as the principal stimulus for this work where we present the results o f a preliminary survey o f the A sianidia species carried out in a patch o f the Madeiran laurel forest. The following is an analysis o f the diversity o f the A sianidia species found and their seasonal variation in abundance during a two-year period, as well as o f the associations between these leafhoppers and their host-plants.

2. Material and Methods

The study was carried out at Chao da Ribeira (32°47’N, 17°06’W) which is located in the northern part o f Madeira island, near Seixal (Fig. 1). Selected plant species o f the upland laurisilva were sampled by standardized sweeping with entomological nets. Sweep netting was followed since besides being an easy and quick method o f sampling terrestrial insects, it had proven in previous studies to be quite effective for surveying A sianidia (e.g., Quartau, 1996; Quartau & Remane, 1996; Quartau et a l 2004). The number of sweeps varied between five and 20, according to the morphological and phenological characteristics o f the individual plant. Sampling took place from May 1997 until June 1999 and was performed monthly, whenever the weather conditions allowed it (during December 1997 sampling was not possible). The data collected during this two-year period were pooled to identify the patterns o f seasonal abundance for the three most common A sianidia species: A . albula,A . decolor and A . insulana.

Fig. 1: Surveying site in Madeira island (dark circle) and Madeiran laurisilva (shaded area). 50 J. A. Quartau et©Arbeitskreis al. Zikaden Mitteleuropas e.V. - download unter www.biologiezentrum.at

The sampling was undertaken on the most characteristic and/or endemic plant species (Neves et a l, 1996; Borges et al., 2008) o f the three main vegetation layers: (a) arboreal layer Ocotea foetens, Taurus novocanariensis, S a lix canariensis, Clethra arborea and Euphorbia mellifera\ (b) arbustive layer nobla, Teucrium betonicum, Argyranthemum pinnatijidum, Erica platycodon, Rubio agostinhoi, Bystropogon maderensis and Heberdenia excelsa\ and (c) herbaceous layer Teline madeirensis, Festuca donax, Geranium palmatum, Cedronella canariensis, Oenanthe divaricata and Erigeron karvinskianus.

Further plant species, not referred to above, have also been sampled during this period, but no specimens of A sianidia were obtained from them. The present study follows the species interpretation within A sianidia of Lindberg (1954, 1961), Quartau (1996) and Quartau & Remane (1996). The Index of Levins (LO) was applied to the data on insect-plant associations for selected A sianidia species in order to evaluate the degree o f overlap of their plant preferences (Levins, 1968; Ludwig & Reynolds, 1988).

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3. Results

During this study five A sianidia species were found, namely A . albula, A . decolor, A . insulana, A . chysanthemi and A . melliferae. More than five hundred specimens were captured as a result o f the two-year sampling period (Table I). A sianidia decolor was the most abundant species (47%), followed by A . albula (36%) and A . insulana (16%). Only three specimens of A . chysanthemi were sampled during the surveying period. All were found on Argyranthemum pinnatijidum, which is in accordance with previous findings indicating that A . pinnatijidum is the host-plant o f this leafhopper both for feeding and ovipositing (Quartau, 1996). On the other hand, A sianidia melliferae was recorded only once and the very one specimen collected was found on Euphorbia mellifera, which is also in accordance with previous ecological data for this species (Quartau, 1996). A . albula appeared to be the most generalist species. It was collected on 13 different plant species and was present in all three vegetation layers (Table I). Besides occurring predominantly in the herbaceous layer, this species presented a strong association with Cedronella canariensis (Fig. 2). On the other hand, A . decolor and A . insulana appeared to be oligophagous species since they were found on several plant species (Table 1), being the former present in great numbers in the canopy of Salix canariensis (Fig. 3). A . insulana appeared to be especially associated with Kubia agostinhoi (Fig. 4). In order to quantify the degree of host plant overlap between the most common species of A sianidia, Levins index of overlap (Lo) was calculated for the following pairs of species: A . albula - A . decolor and A . albula - A . insulana. This procedure was not applied to A . decolor and. A . insulana because they did not share any host-plants (Fig. 5). The results of this analysis indicated that there is a considerable overlap between A . albula and A . decolor (Lo (alb-dec) = 0.971, Lo (dec-alb) = 0.217). On the contrary, the overlap between A. albula and A . insulana was very small (Lo (alb-ins) = 0.001, Lo (ins-alb) = 0.005). Asianidia©Arbeitskreis Zachvatkin Zikaden Mitteleuropas associated e.V. with - download the laurisilva unter www.biologiezentrum.at forest of Madeira island 51

Table 1: Number of specimens of the three most abundant Asianidia species (A. albula, A . decolor and A . insulana) collected on selected plant species of the Madeiran laurisilva.

Layer Plant species A. albula A. decolor A. insulana Arboreal Clethra arborea 1 0 0 Euphorbia mellifera 0 0 1 Laurus novocanariensis 1 4 0 Ocotea foetens 5 0 1 Salix canariensis 43 223 0 Arbustive Bystropogon maderensis 10 0 0 Erica platycodon 1 0 0 Heberdenia excelsa 9 0 0 Phyllis nobla 2 0 0 Rubia agostinhoi 0 0 52 Teucrium betonicum 4 0 0 Herbaceous Cedronella canariensis 97 15 0 Erigeron karvinskianus 0 0 13 Festuca donax 1 0 6 Geranium palmatum 1 0 10 Oenanthe divaricata 8 0 0 Teline madeirensis 0 1 0 Total relative abundance 183 243 83 Total host species 13 4 6

The three most common A sianidia species were more abundant in spring and summer as expected (Table 2). However, for A . albula and A . decolor a peak o f abundance was also recorded in November. No specimens (both nymphs and adults) were found during the winter months.

Table 2: Seasonal variation of the abundance of three Asianidia species in Madeiran laurisilva. (white: no specimens; light grey: < 5 specimens, dark gray: < 25 specimens, black: > 25 specimens). 52 J. A. Quartau et©Arbeitskreis al. Zikaden Mitteleuropas e.V. - download unter www.biologiezentrum.at

30

10 - a) C.arborea L. novocanariemis 0. fcetens S.canarim

4-0 30

20 -

10 - b) E. platycodon H. exceisa P nobla T bsionlcum

50 n

40 -

10 -

C. canariemt F donax G paimatim 0. divaricata

Hmaies yfemales iiinymphs

Fig. 2: Number of A . albula specimens collected on different plant species of the arboreal (a), arbustive (b) and herbaceous layers (c) of the Madeiran laurisilva. Asianidia©Arbeitskreis Zachvatkin Zikaden Mitteleuropas associated e.V. with - download the laurisilva unter www.biologiezentrum.at forest of Madeira island 53

180 150

120 - 90 - 60 - 30 -

0 L. novocanariensis S. canariensis T. madeirensis C. canariensis

Simales ¡¿females a nymphs

Fig. 3: Number of A . decolor specimens collected on plant species of the arboreal ([Laurus novocanariensis, Salix canariensis) and herbaceous layers feline madeirensis, Cedronella canariensis) of the Madeiran laurisilva.

E. mellifera O. foetens E. katvinskianus F. donax O. palmaium R. agoslinhoi

H males y females w nymphs Fig. 4: Number of A . insulana specimens collected on plant species of the arboreal (Euphorbia mellifera, Ocotea foetens) and herbaceous layers (Erigeron kamnskianus, Festuca donax, Geranium palmatum, Rubia agostinhoi) of the Madeiran laurisilva.

4. Discussion

The present investigation revealed new plant associations within leafhoppers of the genus Asianidia in the Madeiran laurisilva (cf. Quartau, 1996). For the three most abundant Asianidia species it was possile to improve our knowledge on the range of their host- plants. A . albula was recorded for the first time on plants of the genera Clethra, haunts, Ocotea, Bjstropogon, Erica, Heberdenia, Phyllis, Teucrium, Festuca, Geranium and Oenanthe. On the other hand, A . decolor was found for the first time on Laurus and Teline. Moreover, A. tnsulana was collected for the first time on plants o f the genera Euphorbia, Ocotea, Rubio, Erigeron and Festuca. 54 J. A. Quartau et©Arbeitskreis al. Zikaden Mitteleuropas e.V. - download unter www.biologiezentrum.at A.insulana A. decolor

A. albula

Fig. 5 - Host-plant species’ overlap between the three most abundant Asianidia species (A. albula, A. decolor and A . insulana) of the Madeiran laurisilva.

Flowever, it is important to correcdy discriminate between true insect-plant associations and casual occurrences. The presence of nymphs on a particular plant species is usually a clear indication o f a true association since these immature forms have developed from eggs oviposited on it, have limited mobility and usually feed on the same plants used by adults. On the other hand, the record of a few adult specimens on a particular plant species is not indicative o f a true insect-plant association since such occurrences can be incidental. A closer inspection o f our results (cf. Table I) seems to suggest that the ocurrence o f A . albula on plants o f the genera Clethra, l^aurus, Erica, Phyllis, Festuca and Geranium is probably accidental and not an indication o f a real association. The same reasoning can be applied to A . decolor in what concerns its association with Teline, and A . insulana in relation to Euphorbia and Ocotea species. Adults and nymphs o f all three A sianidia species were common on their host-plants during spring and summer Both A . albula and A . decolor showed another peak of abundance in November, suggesting that these two species may be bivoltine. The absence of specimens during winter makes us suppose that in these species overwintering occurs mostly in the egg stage. The analysis of the trophic spectra o f the three most abundant A sianidia species show some overlap on their host-plant species. A . insulana and A . decolor do not share host-plant species, but both of these species exhibit some degree of overlap with A . albula (Fig. 5). The high degree of overlap found between A . albula and A . decolor contrasts with the one found between A . albula and A . insulana (a Lo o f about 0.97 as against 0.22, respectively). This finding is possibly a reflection of the phylogenetical proximity between the former pair of species (Lindberg, 1954, 1961; Quartau, 1996). A . decolor and A . albula both belong to the apiculata species group and it is possible that one species has derived from the other Asianidia©Arbeitskreis Zachvatkin Zikaden Mitteleuropasassociated e.V. with - download the laurisilva unter www.biologiezentrum.at forest of Madeira island 55

by the colonization of different hosts. Besides being morphologically similar, these species still maintain similar trophic spectra probably as a result of biological constraints determined by their close gene pools. Although plausible, this hypothesis needs support from accurate molecular phylogenies. On the other hand, A . insulana has distinct host- plants from those recorded for A . albula and A . decolor. A . insulana belongs to a different species group — theperspicillata complex - and is also morphologically different, presenting distinctive dark patterning on the head, thorax and elytra (Quartau, 1996) which may confer some ecological advantage (e.g., predator avoidance). In conclusion we would like to emphasize the need for further studies on the interactions between these A sianidia species and their host-plants, namely their possible origin through radiation in Madeira (and the Canaries) by progressive adaptation to different host-species. On the other hand, the biosystematic affinities within A sianidia are still poorly understood and the taxonomic status o f particular populations is still unclear. As such, further investigations should be carried out with a view to identify and describe the entire diversity o f host-plants, as well as the outlines o f the life histories o f these species, namely the number o f generations per year and the stage in which they overwinter.

5. Acknowledgements

This work was supported by Fundaq:ao para a Ciencia e a Tecnologia (Project PRAXIS/2/2.1/BIA/283/94) and Centro de Biologia Ambiental (Universidade de Lisboa). CR was supported by project research grants GGPXXI/BIC and BPD/66934/2009. DM, MB and YG were supported by research grants (GGPXXI/BIC) from Fundac;ao para a Ciencia e a Tecnologia. The authors are especially grateful to Isamberto Silva, Fernando Nunes and Fernando Maurilio for their help during fieldwork. For facilities in the field we also acknowledge Dora Aguin-Pombo.

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